Autoantibodies in movement and psychiatric disorders: Updated concepts in detection methods, pathogenicity, and CNS entry

Annals of the New York Academy of Sciences

Volumn 1351, Issue 1, 2015, Pages 22-38

  Sinmaz, Nese ^a   Amatoury, Mazen ^a   Merheb, Vera ^a   Ramanathan, Sudarshini ^a   Dale, Russell C ^a,b   Brilot, Fabienne ^a,b  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Anti NMDAR encephalitis; Autoantibodies; Autoimmune encephalitis; Basal ganglia encephalitis; Movement disorder; Psychosis

Indexed keywords

AUTOANTIBODY;

ALLERGIC ENCEPHALITIS; ANTI N METHYL D ASPARTATE RECEPTOR ENCEPHALITIS; ANTIBODY DETECTION; ARTICLE; AUTOIMMUNE DISEASE; BASAL GANGLIA ENCEPHALITIS; BLOOD BRAIN BARRIER; CELL ASSAY; CENTRAL NERVOUS SYSTEM; CEREBROSPINAL FLUID LEVEL; CHOREA MINOR; CLINICAL FEATURE; EXTRAPYRAMIDAL SYNDROME; GOLD STANDARD; HUMAN; IMMUNOASSAY; MENTAL DISEASE; MOTOR DYSFUNCTION; NONHUMAN; PATHOGENICITY; SCHIZOPHRENIA; AUTOIMMUNE DISEASES; BLOOD; CHOREA; IMMUNOLOGY; IMMUNOTHERAPY; PATHOLOGY; PROCEDURES; PSYCHOLOGY; PSYCHOTIC DISORDERS;

ANTI-N-METHYL-D-ASPARTATE RECEPTOR ENCEPHALITIS; AUTOANTIBODIES; AUTOIMMUNE DISEASES; BASAL GANGLIA DISEASES; CHOREA; HUMANS; IMMUNOTHERAPY; PSYCHOTIC DISORDERS; SCHIZOPHRENIA;

EID: 84941811388     PISSN: 00778923     EISSN: 17496632     Source Type: Journal    
DOI: 10.1111/nyas.12764     Document Type: Article

References (100)

1. Lancaster, E. & J. Dalmau 2012. Neuronal autoantigens-pathogenesis, associated disorders and antibody testing. Nat. Rev. Neurol. 8: 380-390.
2. Vincent, A. et al. 2011. Autoantibodies associated with diseases of the CNS: new developments and future challenges. Lancet Neurol. 10: 759-772.
3. Titulaer, M.J. et al. 2013. Treatment and prognostic factors for long-term outcome in patients with anti-NMDA receptor encephalitis: an observational cohort study. Lancet Neurol. 12: 157-165.
4. McKeon, A. & S.J. Pittock 2011. Paraneoplastic encephalomyelopathies: pathology and mechanisms. Acta Neuropathol. 122: 381-400.
5. Bien, C.G. et al. 2012. Immunopathology of autoantibody-associated encephalitides: clues for pathogenesis. Brain 135: 1622-1638.
6. Zuliani, L. et al. 2012. Central nervous system neuronal surface antibody associated syndromes: review and guidelines for recognition. J. Neurol. Neurosurg. Psychiatry 83: 638-645.
7. Ramanathan, S. et al. 2013. Autoimmnue encephalitis: recent updates and emerging challenges. J. Clin. Neurosci. 21: 722-730.
8. Irani, S.R. et al. 2014. Cell-surface central nervous system autoantibodies: clinical relevance and emerging paradigms. Ann. Neurol. 76: 168-184.
9. Dalmau, J. et al. 2007. Paraneoplastic anti-N-methyl-D-aspartate receptor encephalitis associated with ovarian teratoma. Ann. Neurol. 61: 25-36.
10. Lancaster, E. et al. 2010. Antibodies to the GABA(B) receptor in limbic encephalitis with seizures: case series and characterisation of the antigen. Lancet Neurol. 9: 67-76.
11. Petit-Pedrol, M. et al. 2014. Encephalitis with refractory seizures, status epilepticus, and antibodies to the GABAA receptor: a case series, characterisation of the antigen, and analysis of the effects of antibodies. Lancet Neurol. 13: 276-286.
12. Lai, M. et al. 2009. AMPA receptor antibodies in limbic encephalitis alter synaptic receptor location. Ann. Neurol. 65: 424-434.
13. Irani, S.R. et al. 2010. Antibodies to Kv1 potassium channel-complex proteins leucine-rich, glioma inactivated 1 protein and contactin-associated protein-2 in limbic encephalitis, Morvan's syndrome and acquired neuromyotonia. Brain 133: 2734-2748.
14. Lai, M. et al. 2010. Investigation of LGI1 as the antigen in limbic encephalitis previously attributed to potassium channels: a case series. Lancet Neurol. 9: 776-785.
15. Lancaster, E. et al. 2011. Investigations of caspr2, an autoantigen of encephalitis and neuromyotonia. Ann. Neurol. 69: 303-311.
16. Boronat, A. et al. 2013. Encephalitis and antibodies to dipeptidyl-peptidase-like protein-6, a subunit of Kv4.2 potassium channels. Ann. Neurol. 73: 120-128.
17. Hutchinson, M. et al. 2008. Progressive encephalomyelitis, rigidity, and myoclonus: a novel glycine receptor antibody. Neurology 71: 1291-1292.
18. Lancaster, E. et al. 2011. Antibodies to metabotropic glutamate receptor 5 in the Ophelia syndrome. Neurology 77: 1698-1701.
19. Dale, R.C. et al. 2012. Antibodies to surface dopamine-2 receptor in autoimmune movement and psychiatric disorders. Brain 135: 3453-3468.
20. Saiz, A. et al. 1999. Anti-amphiphysin I antibodies in patients with paraneoplastic neurological disorders associated with small cell lung carcinoma. J. Neurol. Neurosurg. Psychiatry 66: 214-217.
21. Saiz, A. et al. 2008. Spectrum of neurological syndromes associated with glutamic acid decarboxylase antibodies: diagnostic clues for this association. Brain 131: 2553-2563.
22. Amatoury, M. 2013. High-throughput flow cytometry cell-based assay to detect antibodies to N-Methyl D-Aspartate receptor or Dopamine-2 receptor in human serum. J. Vis. Exp. 81: e50935.
23. Dale, R.C. et al. 2014. Antibodies to MOG have a demyelination phenotype and affect oligodendrocyte cytoskeleton. Neurol. Neuroimmunol. Neuroinflamm. 1: e12.
24. Mohammad, S.S. et al. 2014. Herpes simplex encephalitis relapse with chorea is associated with autoantibodies to N-Methyl-D-aspartate receptor or dopamine-2 receptor. Mov. Disord. 29: 117-122.
25. Pathmanandavel, K. et al. 2015. Antibodies to surface dopamine-2 receptor and N-methyl-d-aspartate receptor in the first episode of acute psychosis in children. Biol. Psychiatry 77: 537-547.
26. Dale, R.C. et al. 2009. N-methyl-D-aspartate receptor antibodies in pediatric dyskinetic encephalitis lethargica. Ann. Neurol. 66: 704-709.
27. Dalmau, J. et al. 2008. Anti-NMDA-receptor encephalitis: case series and analysis of the effects of antibodies. Lancet Neurol. 7: 1091-1098.
28. Leypoldt, F., T. Armangue & J. Dalmau 2015. Autoimmune encephalopathies. Ann. N.Y. Acad. Sci. 1338: 94-114.
29. Titulaer, M.J., M.S. Kayser & J. Dalmau 2013. Prevalence and treatment of anti-NMDA receptor encephalitis. Lancet Neurol. 12: 425-426.
30. Florance, N.R. et al. 2009. Anti-N-methyl-D-aspartate receptor (NMDAR) encephalitis in children and adolescents. Ann. Neurol. 66: 11-18.
31. Mohammad, S.S. et al. 2014. Movement disorders in children with anti-NMDAR encephalitis and other autoimmune encephalopathies. Mov. Disord. 29: 1539-1542.
32. Dalmau, J. et al. 2011. Clinical experience and laboratory investigations in patients with anti-NMDAR encephalitis. Lancet Neurol. 10: 63-74.
33. Day, G.S. et al. 2014. Abnormal neurons in teratomas in NMDAR encephalitis. JAMA Neurol. 71: 717-724.
34. Armangue, T. et al. 2013. Pediatric anti-N-methyl-D-aspartate receptor encephalitis-clinical analysis and novel findings in a series of 20 patients. J. Pediatr. 162: 850-856, e852.
35. Hacohen, Y. et al. 2014. N-methyl-D-aspartate receptor antibodies in post-herpes simplex virus encephalitis neurological relapse. Mov. Disord. 29: 90-96.
36. Oldstone, M.B. 1998. Molecular mimicry and immune-mediated diseases. FASEB J. 12: 1255-1265.
37. Dale, R.C. et al. 2004. Encephalitis lethargica syndrome: 20 new cases and evidence of basal ganglia autoimmunity. Brain 127: 21-33.
38. Irani, S.R. et al. 2011. Faciobrachial dystonic seizures precede Lgi1 antibody limbic encephalitis. Ann. Neurol. 69: 892-900.
39. Andrade, D.M. et al. 2011. Tonic seizures: a diagnostic clue of anti-LGI1 encephalitis? Neurology 76: 1355-1357.
40. Striano, P., V. Belcastro & S. Striano 2011. Tonic seizures: a diagnostic clue of anti-LGI1 encephalitis? Neurology 77: 2140; author reply: 2141-2143.
41. Meinck, H.M. & P.D. Thompson 2002. Stiff man syndrome and related conditions. Mov. Disord. 17: 853-866.
42. Stern, W.M. et al. 2014. Glycine receptor antibody mediated Progressive Encephalomyelitis with Rigidity and Myoclonus (PERM): a rare but treatable neurological syndrome. Pract. Neurol. 14: 123-127.
43. Damasio, J. et al. 2013. Progressive encephalomyelitis with rigidity and myoclonus: the first pediatric case with glycine receptor antibodies. JAMA Neurol. 70: 498-501.
44. Mas, N. et al. 2011. Antiglycine-receptor encephalomyelitis with rigidity. J. Neurol. Neurosurg. Psychiatry 82: 1399-1401.
45. Kruer, M.C. et al. 2014. Aggressive course in encephalitis with opsoclonus, ataxia, chorea, and seizures: the first pediatric case of gamma-aminobutyric acid type B receptor autoimmunity. JAMA Neurol. 71: 620-623.
46. Suleiman, J. et al. 2013. Autoantibodies to neuronal antigens in children with new-onset seizures classified according to the revised ILAE organization of seizures and epilepsies. Epilepsia 54: 2091-2100.
47. Hacohen, Y. et al. 2014. Autoantibody biomarkers in childhood-acquired demyelinating syndromes: results from a national surveillance cohort. J. Neurol. Neurosurg. Psychiatry 85: 456-461.
48. Hacohen, Y. et al. 2013. Paediatric autoimmune encephalopathies: clinical features, laboratory investigations and outcomes in patients with or without antibodies to known central nervous system autoantigens. J. Neurol. Neurosurg. Psychiatry 84: 748-755.
49. Ribeiro, P.A. et al. 2008. Expression profile of Lgi1 gene in mouse brain during development. J. Mol. Neurosci. 35: 323-329.
50. Kirvan, C.A. et al. 2003. Mimicry and autoantibody-mediated neuronal cell signaling in Sydenham chorea. Nat. Med. 9: 914-920.
51. Cardoso, F. et al. 1997. Chorea in fifty consecutive patients with rheumatic fever. Mov. Disord. 12: 701-703.
52. Brilot, F. et al. 2011. Antibody binding to neuronal surface in Sydenham chorea, but not in PANDAS or Tourette syndrome. Neurology 76: 1508-1513.
53. Brimberg, L. et al. 2012. Behavioral, pharmacological, and immunological abnormalities after streptococcal exposure: a novel rat model of Sydenham chorea and related neuropsychiatric disorders. Neuropsychopharmacology 37: 2076-2087.
54. Church, A.J. et al. 2002. Anti-basal ganglia antibodies in acute and persistent Sydenham's chorea. Neurology 59: 227-231.
55. Kirvan, C.A. et al. 2007. Tubulin is a neuronal target of autoantibodies in Sydenham's chorea. J. Immunol. 178: 7412-7421.
56. Rhoads, J. et al. 2011. Lack of anti-NMDA receptor autoantibodies in the serum of subjects with schizophrenia. Schizophr. Res. 129: 213-214.
57. Chang, K. et al. 2015. Clinical Evaluation of Youth with Pediatric Acute-Onset Neuropsychiatric Syndrome (PANS): recommendations from the 2013 PANS consensus conference. J. Child Adolesc. Psychopharmacol. 25: 3-13.
58. Swedo, S.E. et al. 1998. Pediatric autoimmune neuropsychiatric disorders associated with streptococcal infections: clinical description of the first 50 cases. Am. J. Psychiatry 155: 264-271.
59. Laruelle, M. 2014. Schizophrenia: from dopaminergic to glutamatergic interventions. Curr. Opin. Pharmacol. 14: 97-102.
60. Coutinho, E., P. Harrison & A. Vincent 2014. Do neuronal autoantibodies cause psychosis? A neuroimmunological perspective. Biol. Psychiatry 75: 269-275.
61. Rothermundt, M., V. Arolt & T.A. Bayer 2001. Review of immunological and immunopathological findings in schizophrenia. Brain Behav. Immun. 15: 319-339.
62. Miller, B. J. et al. 2011. Meta-analysis of cytokine alterations in schizophrenia: clinical status and antipsychotic effects. Biol. Psychiatry 70: 663-671.
63. Ezeoke, A. et al. 2013. A systematic, quantitative review of blood autoantibodies in schizophrenia. Schizophr. Res. 150: 245-251.
64. Steiner, J. et al. 2013. Increased prevalence of diverse N-methyl-D-aspartate glutamate receptor antibodies in patients with an initial diagnosis of schizophrenia: specific relevance of IgG NR1a antibodies for distinction from N-methyl-D-aspartate glutamate receptor encephalitis. JAMA Psychiatry 70: 271-278.
65. Zandi, M.S. et al. 2011. Disease-relevant autoantibodies in first episode schizophrenia. J. Neurol. 258: 686-688.
66. Pollak, T.A. et al. 2014. Prevalence of anti-N-methyl-D-aspartate (NMDA) receptor antibodies in patients with schizophrenia and related psychoses: a systematic review and meta-analysis. Psychol. Med. 44: 2475-2487.
67. Dahm, L. et al. 2014. Seroprevalence of autoantibodies against brain antigens in health and disease. Ann. Neurol. 76: 82-94.
68. Hammer, C. et al. 2014. Neuropsychiatric disease relevance of circulating anti-NMDA receptor autoantibodies depends on blood-brain barrier integrity. Mol. Psychiatry 19: 1143-1149.
69. Muller, U.J. et al. 2014. Absence of dopamine receptor serum autoantibodies in schizophrenia patients with an acute disease episode. Schizophr. Res. 158: 272-274.
70. Tanaka, S. et al. 2003. Autoantibodies against four kinds of neurotransmitter receptors in psychiatric disorders. J. Neuroimmunol. 141: 155-164.
71. Dale, R.C. et al. 2014. Utility and safety of rituximab in pediatric autoimmune and inflammatory CNS disease. Neurology 83: 142-150.
72. Irani, S.R. et al. 2010. N-methyl-D-aspartate antibody encephalitis: temporal progression of clinical and paraclinical observations in a predominantly non-paraneoplastic disorder of both sexes. Brain 133: 1655-1667.
73. Vincent, A. et al. 2004. Potassium channel antibody-associated encephalopathy: a potentially immunotherapy-responsive form of limbic encephalitis. Brain 127: 701-712.
74. Chang, T. et al. 2013. Immunization against GAD induces antibody binding to GAD-independent antigens and brainstem GABAergic neuronal loss. PLoS One 8: e72921.
75. Fujita, K. et al. 2012. Antibodies to N-methyl-D-aspartate glutamate receptors in Creutzfeldt-Jakob disease patients. J. Neuroimmunol. 251: 90-93.
76. Uzawa, A. et al. 2012. Anti-N-methyl-D-aspartate-type glutamate receptor antibody-positive limbic encephalitis in a patient with multiple sclerosis. Clin. Neurol. Neurosurg. 114: 402-404.
77. Ohshita, T. et al. 2006. Voltage-gated potassium channel antibodies associated limbic encephalitis in a patient with invasive thymoma. J. Neurol. Sci. 250: 167-169.
78. Engelhardt, B. & R.M. Ransohoff 2005. The ins and outs of T-lymphocyte trafficking to the CNS: anatomical sites and molecular mechanisms. Trends Immunol. 26: 485-495.
79. Ransohoff, R.M., P. Kivisakk & G. Kidd 2003. Three or more routes for leukocyte migration into the central nervous system. Nat. Rev. Immunol. 3: 569-581.
80. Hickey, W.F. 2001. Basic principles of immunological surveillance of the normal central nervous system. Glia 36: 118-124.
81. Roopenian, D.C. & S. Akilesh 2007. FcRn: the neonatal Fc receptor comes of age. Nat. Rev. Immunol. 7: 715-725.
82. Lossinsky, A.S. & R.R. Shivers 2004. Structural pathways for macromolecular and cellular transport across the blood-brain barrier during inflammatory conditions. Histol. Histopathol. 19: 535-564.
83. Scott, G.S. et al. 2007. Glutamate-stimulated peroxynitrite production in a brain-derived endothelial cell line is dependent on N-methyl-D-aspartate (NMDA) receptor activation. Biochem. Pharmacol. 73: 228-236.
84. Broadwell, R.D. & M.V. Sofroniew 1993. Serum proteins bypass the blood-brain fluid barriers for extracellular entry to the central nervous system. Exp. Neurol. 120: 245-263.
85. Redzic, Z. 2011. Molecular biology of the blood-brain and the blood-cerebrospinal fluid barriers: similarities and differences. Fluids Barriers CNS 8: 3.
86. Carvajal-Gonzalez, A. et al. 2014. Glycine receptor antibodies in PERM and related syndromes: characteristics, clinical features and outcomes. Brain 137: 2178-2192.
87. Nakamura, T. et al. 2014. Distinct motor impairments of dopamine D1 and D2 receptor knockout mice revealed by three types of motor behavior. Front. Integr. Neurosci. 8: 56.
88. Klein, C. et al. 1999. Association of a missense change in the D2 dopamine receptor with myoclonus dystonia. Proc. Natl. Acad. Sci. USA 96: 5173-5176.
89. Hughes, E.G. et al. 2010. Cellular and synaptic mechanisms of anti-NMDA receptor encephalitis. J. Neurosci. 30: 5866-5875.
90. Mikasova, L. et al. 2012. Disrupted surface cross-talk between NMDA and Ephrin-B2 receptors in anti-NMDA encephalitis. Brain 135: 1606-1621.
91. Manto, M. et al. 2011. Afferent facilitation of corticomotor responses is increased by IgGs of patients with NMDA-receptor antibodies. J. Neurol. 258: 27-33.
92. Planaguma, J. et al. 2015. Human N-methyl-D-aspartate receptor antibodies alter memory and behaviour in mice. Brain 138: 94-109.
93. Peng, X. et al. 2015. Cellular plasticity induced by anti-AMPA receptor encephalitis antibodies. Ann. Neurol. 77: 381-398.
94. Mayer, M.C. et al. 2013. Distinction and temporal stability of conformational epitopes on myelin oligodendrocyte glycoprotein recognized by patients with different inflammatory central nervous system diseases. J. Immunol. 191: 3594-3604.
95. Gleichman, A.J. et al. 2012. Anti-NMDA receptor encephalitis antibody binding is dependent on amino acid identity of a small region within the GluN1 amino terminal domain. J. Neurosci. 32: 11082-11094.
96. Gleichman, A.J. et al. 2014. Antigenic and mechanistic characterization of anti-AMPA receptor encephalitis. Ann. Clin. Transl. Neurol. 1: 180-189.
97. Haussleiter, I.S. et al. 2012. Investigation of antibodies against synaptic proteins in a cross-sectional cohort of psychotic patients. Schizophr. Res. 140: 258-259.
98. Masdeu, J.C. et al. 2012. Serum IgG antibodies against the NR1 subunit of the NMDA receptor not detected in schizophrenia. Am. J. Psychiatry 169: 1120-1121.
99. Tsutsui, K. et al. 2012. Anti-NMDA-receptor antibody detected in encephalitis, schizophrenia, and narcolepsy with psychotic features. BMC Psychiatry 12: 37.
100. Doss, S. et al. 2014. High prevalence of NMDA receptor IgA/IgM antibodies in different dementia types. Ann. Clin. Transl. Neurol. 1: 822-832.